Impact of heavy metal stress on plants and the role of various defense elements

Subject Areas : Stress Physiology

Tanveer Bilal Pirzadah ¹ , Bisma Malik ² , Sheikh Tanveer Salam ³ , Pervaiz Ahmad Dar ⁴ , Seema Rashid ⁵

1 - Department of Bioresources, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
2 - Department of Bioresources, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
3 - Department of Zoology, Amar Singh College, Cluster University, Srinagar (J&K)
4 - Department of Zoology, Amar Singh College, Cluster University, Srinagar (J&K)
5 - Department of Zoology, Amar Singh College, Cluster University, Srinagar (J&K)

Received: 2019-11-04 Accepted : 2019-11-04 Published : 2019-08-01

Keywords: ROS, Heavy metals, MAPK pathway, metallothioneins, transcription factors,

Abstract :

Heavy metal (HMs) pollution is currently one of the serious issues for the environment and agriculture as it has a direct impact on the production yield. This situation has gained a rapid momentum in the present era due to the population pressure, industrialization, and various anthropogenic activities which in turn lead to oxidative stress in plants and thus disturbs the redox homeostasis and ultimately affects the crop yield. However, plants possess a different regulatory system that work in a synergetic manner to combat stress and thus adapt themselves in such contaminated soils. These act as sinks to neutralize the toxic effects of these heavy metals by chelation, sequestration, and intensification of enzyme system. Excessive stress induces a cascade, MAPK (mitogen-activated protein kinase) pathway and biosynthesis of metal detoxifying ligands. The understanding of detoxification mechanism of metal ions through MAPK cascade and biosynthesis of metal-detoxifying ligands is an interesting way for searching insights and outlook in the field of plant biotechnology. Here, we discuss the impact of heavy metals on plants and the role of different regulatory elements that play a prominent role in metal detoxification.

References:

Asai, S., K, Ohta and H. Yoshioka.2008. 'MAPK signaling regulates nitric oxide and NADPH oxidase dependent oxidative bursts in Nicotiana benthamiana'. Plant Cell 20: 1390–1406.

Asai, T., G. Tena., J. Plotnikova., M.R. Willmann., W. L. Chiu., L. Gomez-Gomez., T. Boller., F.M. Ausubel and J. Sheen. 2002. 'MAP kinase signaling cascade in Arabidopsis innate immunity'. Nature,415: 977–983.

Ashraf, M.A., I. Hussain., R. Rasheed., M. Iqbal and M. Riaz.2017. 'Advances in microbe-assisted reclamation of heavy metal contaminated soils over the last decade: a review'. J Environ Manag, 198: 132–143.

Backor, M. and S. Loppi. 2009. 'Interactions of lichens with heavy metals'. Biol Plant 53: 214–222.

Ban, Q.Y., G.F. Liu and Y. C. Wang. 2011.' A DREB gene from Limonium bicolor mediates molecular and physiological responses to copper stress in transgenic tobacco'. J Plant Physiol, 168: 449–458.

Barone, L.M., C. Shih and B.P. Wasserman.1997. 'Mercury-induced conformational changes and identification of conserved surface loops in plasma membrane aquaporin’s from higher plants'. J Biol Chem, 272 (49): 30672–30677.

Beaudette, P.C., M. Chlup., J. Yee and R.J. Emery. 2007. 'Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl₂ and ABA'. J Exp Bot 58: 1291–1300.

Berta, M., A. Giovannelli., E. Potenza., M.L. Traversi and M.L. Racchi. 2009. 'Type 3 metallothioneins respond to water deficit in leaf and in the cambial zone of white poplar (Populus alba)'. J Plant Physiol. 166: 521–530.

Blaylock, M.J. and J.W. Huang. 2000. 'Phytoextraction of metals in Phytoremediation of Toxic Metals: Using Plants to clean up the environment'. In: Raskin I, Ensley BD(ed) JohnWiley & Sons, New York, NY, USA, pp 53–71

Cargnelutti, D., L.A. Tabaldi., R. M. Spanevello., G. O. Jucoski., V. Battisti., M. Redin., C.E.B. Linares., V.L. Dressler., M.M. Flores., F. T. Nicoloso., V. M. Morsch and M.R.C. Schetinger. 2006. 'Mercury toxicity induces oxidative stress in growing cucumber seedlings'. Chemosphere 65: 999–1006.

Castiglione, S., C. Franchin., T. Fossati., G. Lingua., P. Torrigiani and S. Biondi. 2007. 'High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba L. cv. Villafranca)'. Chemoshpere. 67: 1117–1126.

Chaumont, F., F. Barrieu., E. Wojcik., M. J. Chrispeels and R. Jung. 2001. 'Aquaporins constitute a large and highly divergent protein family in maize'. Am Soc Plant Physiol. 125: 1206–1215.

Chen, Y.A., W.C. Chi., N.N. Trinh., L.Y. Huang., Y.C. Chen., K.T. Cheng., T.L. Huang, C.Y. Lin and H.J. Huang. 2014. 'Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings'. PLoS ONE 9: e95163.

Chen, Y., S. Wang., Z. Nan., J. Ma and F. Zang. 2017. 'Effect of fluoride and cadmium stress on the uptake and translocation of fluoride and cadmium and other mineral nutrition elements in radish in single element or contaminated sierozem'. Environ Exp Bot.134: 54–61.

Cuypers, A., S. Hendrix., R. Amaral dos Reis., S. De Smet S., J. Deckers., H. Gielen., M. Jozefczak, C. Loix., H. Vercampt., J. Vangronsveld and E. Keunen. 2016. 'Hydrogen Peroxide, Signaling in Disguise during Metal Phytotoxicity'. Front Plant Sci 7:470.

Dalcorso, G., S. Farinati and A. Furini. 2010.'Regulatory networks of cadmium stress in plants. Plant Signal Behav. 5(6): 663–667.

Danielson, J.A.H. and U. Johanson. 2008. 'Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens'. BMC Plant Biol 8: 45.

Das, K., M. Chiranjib., N. Ghosh., S. Banerjee and N. Dey. 2014. 'Effects of exogenous spermidine on cell wall composition and carbohydrate metabolism of Marsilea plants under cadmium stress'. J Plant Physiol Pathol. 2:3.

Das, K., and A. Roychoudhury.2014. 'Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants'. Front Environ Sci. 2:53.

de Araújo, R.P., A.A.F. de Almeida., L.S. Pereira., P.A. Mangabeira., J.O. Souza., C.P. Pirovani., D. Ahnert and V.C. Baligar. 2017. 'Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil'. Ecotoxicol Environ Saf. 144: 148–157.

Demidchik, V. 2018. 'ROS-Activated Ion Channels in Plants: Biophysical Characteristics, Physiological Functions and Molecular Nature. Int J Mol Sci 19(4): 1263-1281.

Dubey, R.S. 2011.'Metal toxicity, oxidative stress and antioxidative defense system in plants In: Gupta SD (ed)Reactive Oxygen Species and Antioxidants in Higher Plants'. CRC Press, Boca Raton, Fla, USA, pp 177–203.

Fusco, N., L. Micheletto., G. Dal Corso., L. Borgato and A. Furini. 2005.'Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L'. J Exp Bot. 421 (56): 3017– 3027.

Gielen, H., J. Vangronsveld and A. Cuypers. 2017. 'Cd-induced Cu deficiency responses in Arabidopsis thaliana: are phytochelatins involved?' Plant Cell Environ,40: 390–400.

Gill, M. 2014. 'Heavy metal stress in plants: a review'. Int J AdvRes 2 (6): 1043-1055.

Gong,B., W. Nie., Y. Yan., Z. Gao and Q. Shi. 2017. 'Unravelling cadmium toxicity and nitric oxide induced tolerance in Cucumis sativus: insight into regulatory mechanisms using proteomics'. J Hazard Mater ,336: 202–213.

González-Guerrero M., V. Escudero., A. Saéz and M. Tejada-Jiménez. 2016. 'Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia'. Front Plant Sci 7: 1088.

Gruenhage, L., and Jager, I.I.J. 1985. 'Effect of heavy metals on growth and heavy metals content of Allium Porrum and Pisum sativum'. Angew Bot 59: 11–28.

Gunse, B., C. Poschenrieder and J. Barcelo. 1997. 'Water transport properties of roots and root cortical cells in proton- and Al stressed maize varieties'. Plant Physiol 113: 595–602.

Guo, J., L. Xu, Y. Su, H. Wang, S. Gao, J. Xu and Y. Que. 2013. 'ScMT2-1-3, a Metallothionein Gene of Sugarcane, Plays an Important Role in the Regulation of Heavy Metal Tolerance/Accumulation'. BioMed Res Int. 904769: 1-12.

Guo, T.R., G.P. Zhang., M. X. Zhou., F.B. Wu and J.K. Chen. 2004. 'Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance'. Plant and Soil 258: 241-248.

Guo, W.J., W. Bundithya and P.B. Goldsbrough. 2003. 'Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper'. New Phytol.159: 369–381.

Hamel, L.P., M.C. Nicole, S. Sritubtim, M.J. Morency, M. Ellis, J. Ehlting, N. Beaudoin , B. Barbazuk, D. Klessig, J. Lee, G. Martin, J. Mundy, Y. Ohashi, D. Scheel, J. Sheen , T. Xing, S. Zhang, A. Seguin and  B.E. Ellis. 2006. 'Ancient signals: comparative genomics of plant MAPK and MAPKK gene families'. Trends Plant Sci 11: 192–198. 

Hänsch, R. and R.R. Mendel. 2009. 'Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl)'. Curr Opin Plant Biol ,12: 259-66.

Hawkes, J.S. 1997. 'What is a Heavy metal'. J Chem Edu, 74: 1369–1374.

Henzler, T., Q. Ye and E. Steudle. 2004. 'Oxidative of water channels (aquaporins) in Chara by hydroxyl radicals'. Plant Cell Environ, 27: 1184–1195.

Hirotaka, Y., F. Hiroyuki., A. Tomohito., O. Akio., N. Tsukasa., M. Koji and N. Satomi. 2010. 'Gene expression analysis in cadmium stressed roots of a low cadmium-accumulating solanaceous plant Solanum torvum'. J Exp Bot, 61(2): 423–437.

Horbowicz, M., H. Debski, W. Wiczkowski., D. Szawara-Nowak., D. Koczkodaj., J. Mitrus and H. Sytykiewicz. 2013. 'The impact of short term exposure to Pb and Cd on flavonoid composition and seedling growth of common buckwheat cultivars'. Pol J Environ Stud, 22(6): 1723-1730.

Hossain, M.A. and M. Fujita. 2010.'Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress'. Physiol Mol. Biol. Plants,16 (1): 19–29.

Hossain, M.A., M. Hasanuzzaman and M. Fujita. 2011.'Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycine betaine is correlated with salt tolerance in mung bean'. Front Agric China.  5 (1): 1–14.

Hossain, M.A., A.K.M.Z. Hossain, T. Kihara, H. Koyama and T. Hara. 2005. 'Aluminum-induced lipid peroxidation and lignin deposition are associated with an increase in H₂O₂ generation in wheat seedlings'. Soil Sci Plant Nutr. 51: 223-230.

Hossain, M.A., J. Piyatida, J. A. Teixeira da Silva and M. Fujita. 2012. 'Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, vol. 2012, Article ID 872875, 37 pages, 2012. https://doi.org/10.1155/2012/872875.

Hu, W., X. Hou, C. Huang, Y. Yan, W. Tie, Z. Ding, Y. Wei, J. Liu, H. Miao, Z. Lu, M. Li, B. Xu, and Z. Jin. 2015. 'Genome-Wide Identification and Expression Analyses of Aquaporin Gene Family during Development and Abiotic Stress in Banana'. Int J Mol Sci. 16: 19728-19751.

Huang, G.Y. and Y.S. Wang. 2010. 'Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress'. Aquat Toxicol, 99: 86–92.

Huang, G.Y, Y.S. Wang, G.G. Ying and A.C. Dang. 2012. 'Analysis of type 2 metallothionein gene from mangrove species (Kandelia candel)'. Trees ,26: 1537–1544.

Israr, M. and S.V. Sahi. 2006.'Antioxidative responses to mercury in the cell cultures of Sesbania drummondii'. Plant Physiol Biochem. 44 (10): 590–595.

Jalmi, S.K. and A.K. Sinha. 2015. 'ROS mediated MAPK signaling in abiotic and biotic stress-striking similarities and differences'. Front Plant Sci. 6:769.

Jia, D.U., Y.J. Li and L.I. Cheng-Hao. 2012. 'Advances in metallotionein studies in forest trees'. POJ, 5(1): 46-51.

Johanson, U., M. Karlsson, I. Johansson, S. Gustavsson, S. Sjövall, L. Fraysse, A.R. Weig and P. Kjellbom. 2001. 'The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants'. Plant Physiol.126: 1358–1369.

Jonak, C., H. Nakagami and H. Hirt. 2004. 'Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium'. Plant Physiol. 136: 3276–3283.

Jones, D.L., E.B. Blancaflor, L.V. Kochian and S. Gilroy. 2006. 'Spatial coordination of aluminum uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots'. Plant Cell Environ. 29: 1309-1318.

Jones, D.L., S. Gilroy, P.B.  Larsen, S.H. Howell and L.V. Kochian.1998. 'Effect of aluminum on cytoplasmic Ca²⁺ homeostasis in root hairs of Arabidopsis thaliana'. Planta, 206: 378-387.

Juwarkar, A.S. and G.B. Shende. 1986. 'Interaction of Cd-Pb effect on growth yield and content of Cd, Pb in barley'. Ind J Environ Heal 28: 235–243.

Kagi, J.H.R. 1991. 'Overview of metallothioneins. Methods Enzymol.205: 613–626.

Kammerloher, W., U. Fischer, G.P. Piechotta and A.R. Schäffner. 1994.' Water channels in the plant plasma membrane cloned by immuno-selection from an expression system'. Plant J. 6: 187–199.

Karlsson, M., I. Johansson, M. Bush, M.C. McCann, C. Maurel and C. Larsson. 2000. 'An abundant TIP expressed in mature highly vacuolated cells'. Plant J. 21: 83–90.

Kholodova, V., K. Volkov, A. Adbeyeva and V. Kuznetsov. 2011. 'Water status in Mesembryanthemum crystallinum under heavy metal stress'. Environ. Exp. Bot. 71: 382-389.

Kohler, A., D. Blaudez, M. Chalot, and F. Martin. 2004. 'Cloning and expression of multiple metallothioneins from hybrid poplar'. New Phytol ,164: 83–93.

Korenkov, V., S. H. Park, N.H. Cheng, C. Sreevidya, J. Lachmansingh, J. Morris, K. Hirschi and G.J. Wagner.2007. 'Enhanced Cd²⁺ selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers'. Planta, 225: 403–411.

La Rocca, N., C. Andreoli, G.M. Giacometti, N. Rascio ans I. Moro. 2009. 'Responses of the Antarctic microalga Koliella antartica (Trebouxiophyceae, Chlorophyta) to cadmium contamination'. Photosynthetica, 47, 471–479.

Lee, J., D. Shim, W.Y. Song, I. Hwang and Y. Lee. 2004. 'Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells'. Plant Mol Biol,54: 805–815.

Lee, M., K. Lee, J. Lee, E.W. Noh and Y. Lee. 2005. 'AtPDR12 contributes to lead resistance in Arabidopsis'. Plant Physiol. 138: 827–836.

Leszczyszyn, O.I., H.T. Imam and C.A. Blindauer. 2013. 'Diversity and distribution of plant metallothioneins: A review of structure, properties and functions'. Metallomics, 5(9): 1146–1169.

Levin, M., N. Resnick, Y. Rosianskey, I. Kolotilin, S. Wininger, J. H. Lemcoff, S. Cohen, G. Galili, H. Koltai and Y. Kapulnik.2009. 'Transcriptional profiling of Arabidopsis thaliana plants response to low relative humidity suggests a shoot-root communication'. Plant Sci.177: 450–459.

Lionetto, M.G, R. Caricato, A. Calisi, M.E. Giordano, E. Erroi and T. Schettino.2016. 'Biomonitoring of water and soil quality: a case study of ecotoxicological methodology application to the assessment of reclaimed agro-industrial wastewaters used for irrigation'. Rend Fis Acc Lincei,27:105–112.

Liu, D., X. Wang, Z. Chen, H. Xu and Y. Wang. 2010. 'Influence of mercury on chlorophyll content in winter wheat and mercury bioaccumulation'. Plant Soil Environ. 56: 139–143.

Liu, Q., J.L. Yang, L.S. He, Y.Y. Li and S.J. Zheng. 2008. 'Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale'. Biologia Plantarum 52: 87-92.

Lopez, D., G. Bronner, N. Brunel, D. Auguin, S. Bourgerie, F. Brignolas, S. Carpin, C. Tournaire-Roux, C. Maurel and B. Fumanal. 2012. 'Insights into Populus XIP aquaporins: Evolutionary expansion, protein functionality, and environmental regulation'. J Exp Bot. 63: 2217–2230.

Lu, Y., X. Deng, L. Quan, Y. Xia and Z. Shen. 2015. 'Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana'. Plant Soil, 367: 507–519.

Ma, J.F., S.J. Zheng, S. Hiradate and H. Matsumoto. 1997. 'Detoxifying aluminum with buckwheat'.  Nature, 390: 569–570.

MAPK Group. 2002. 'Mitogen-activated protein kinase cascades in plants: a new nomenclature'. Trends Plant Sci. 7: 301–308.

Mayerová, M., S, Petrová, M. Madaras, J. Lipavský and T. Šimon. 2017. 'Non enhanced phytoextraction of cadmium, zinc, and lead by high yielding crops'. Environ Sci Pollut Res. 24: 14706–14716.

Meharg, A.A. 1993.'The role of plasmalemma in metal tolerance in angiosperm'. Physiologia Plantarum. 88 (1): 191–198.

Mendoza-Cózatl, D.G., T.O. Jobe, F. Hauser, and J. I. Schroeder. 2011. 'Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic'. Curr Opin Plant Biol. 14: 554–562.

Nagata, T. 2014.'Expression analysis of new Metallothionein2-like protein under mercury stress in tomato seedling'. Plant Root, 8: 72-81.

Nakagami, H., A. Pitzschke and H. Hirt. 2005. 'Emerging MAP kinase pathways in plant stress signaling'. Trends Plant Sci. 10: 339–346.

Nevo, Y. and N, Nelson. 2006. 'The NRAMP family of metal-ion transporters'. Biochimica et Biophysica Acta 1763: 609–620.

Nielsen, H.D., M.T. Brown and C. Brownlee. 2003.' Cellular responses of developing Fucus serratus embryos exposed to elevated concentrations of Cu^2+'. Plant Cell Environ. 26: 1737–1747.

Panda, S.K., L.B. Singha and M.H. Khan. 2003. 'Does aluminium phytotoxicity induce oxidative stress in green gram (Vigna radiata)?' Bulgarian Journal of Plant Physiology, 29: 77-86.

Peng, J.S, G. Ding, S. Meng, H.Y. Yi and J.M. Gong. 2017. 'Enhanced metal tolerance correlates with heterotypic variation in SpMTL, a metallothionein-like protein from the hyperaccumulator Sedum plumbizincicola'. Plant Cell Environ, 40(8): 1368-1378.

Peng, J.S. and J.M. Gong. 2014. 'Vacuolar sequestration capacity and long-distance metal transport in plants'. Front Plant Sci.5:19.

Pirzadah, T.B., B. Malik, I. Tahir, M. Kumar, A. Varma and R.U. Rehman. 2014. 'Phytoremediation: An Eco-Friendly Green Technology for Pollution Prevention, Control and Remediation'. In: Hakeem KR, Sabir M, Ozturk M, Mermut AH (ed), Soil Remediation and plants: Prospects and Challenges, Elsevier publications, USA, pp, 107-122.

Pirzadah, T.B., B. Malik, I. Tahir, Q.M. Irfan and R.U. Rehman. 2018. 'Characterization of mercury-induced stress biomarkers in Fagopyrum tataricum plants'. Int J Phytoremediation, 20 (3): 225-236.

Poschenrieder and J. Barcelo. 2004.'Water relations in heavy metal stressed plants'. In: Prasad MNV (ed), Heavy Metal Stress in Plants3^rd eds Springer, Berlin, Germany, pp 249–270.

Pourrut, B., M. Shahid, C. Dumat, P. Winterton and E. Pinelli. 2011. 'Lead Uptake, Toxicity, and Detoxification in Plants'. Rev Environ Contam Toxicol 213: 113-136.

Przedpelska-Wasowicz, E.M. and E. Wierzbicka. 2011. 'Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells'. Protoplasma, 248: 663–671.

Quintela-Sabarís, C., L. Marchand, P.S. Kidd, W. Friesl-Hanl, M. Puschenreiter, J. Kumpiene , I. Müller, S. Neu, J. Janssen, J. Vangronsveld, I. Dimitriou, G. Siebielec, R. Gałązka, V. Bert, R. Herzig, A.B. Cundy, N. Oustrière, A. Kolbas, W. Galland, and M. Mench. 2017. 'Assessing phytotoxicity of trace element-contaminated soils phytomanaged with gentle remediation options at ten European field trials'. Sci Total Environ.599: 1388–1398.

Rodríguez –Llorente, I.D., P. Pérez-Palacios, B. Doukkali, M.A. Caviedes and E. Pajuelo. 2010. 'Expression of the seed-specific metallothionein mt4a in plant vegetative tissues increases Cu and Zn tolerance'. Plant Sci.178: 327–332.

Roos, W., S. Evers, M. Hieke, M. Tschöpe and B. Schumann. 1998.'Shifts of intracellular pH distribution as a part of the signal mechanism leading to the elicitation of benzophenanthridine alkaloids - Phytoalexin biosynthesis in cultured cells of Eschscholtzia californica'. Plant Physiol. 118: 349–364.

Roosens, N.H., C. Bernard, R. Leplae and N. Verbruggen. 2004. 'Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens.' FEBS Lett. 577: 9–16.

Salt, D.E. and W.E. Rauser. 1995. 'MgATP-dependent transport of phytochelatins across the tonoplast of oat roots'. Plant Physiol.107: 1293–1301.

Salt, D.E. and G.J. Wagner. 1993. 'Cadmium transport across tonoplast of vesicles from oat roots. Evidence for a Cd²⁺/H⁺ antiport activity'. J Biol Chem. 268: 12297–12302.

Samardzic, J.T., D.B. Nikloic, G.S. Timotijevic, Z.S. Jovanovic, M.D. Milisavljevic and V.R. Maksimaic. 2010. 'Tissue expression analysis of FeMT3, a drought and oxidative stress related metallothionein gene from buckwheat (Fagopyrum esculentum)'. J Plant Physiol. 167: 1407-1411.

Santi, S. and W. Schmidt. 2009. 'Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots'. New Phytol. 183: 1072–1084.

Savage, D.F. and R.M. Stroud. 2007. 'Structural basis of aquaporin inhibition by mercury'. J Mol Biol. 368 (3): 607–617.

Schmidt, U.G., A. Endler, S. Schelbert, A. Brunner, M. Schnell, H.E. Neuhaus, D. Marty-Mazars, F. Marty, S. Baginsky and E. Martinoia. 2007.'Novel Tonoplast Transporters Identified Using a Proteomic Approach with Vacuoles Isolated from Cauliflower Buds'. Plant Physiol. 145(1): 216–229.

Schutzendubel, A. and A. Polle. 2002.'Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization'. J Exp Bot. 372 (53): 1351–1365.

Sekhar, K., B. Priyanka, V.D. Reddy and K.V. Rao. 2011. 'Metallothionein 1 (CcMT1) of pigeonpea (Cajanus cajan, L.) confers enhanced tolerance to copper and cadmium in Escherichia coli and Arabidopsis thaliana'. Environ Exp Bot.72: 131–139.

Seth, C.S., T. Remans, E. Keunen, M. Jozefczak, H. Gielen, K. Opdenakker, N. Weyens, J. Vangronsveld and A. Cuypers. 2012.'Phytoextraction of toxic metals: a central role for glutathione'. Plant Cell Environ.35 (2): 334–346.

Sharma, P. and R.S. Dubey. 2005. 'Lead toxicity in plants'. Braz J Plant Physiol. 17 (1): 35–52.

Sharma, P. and R.S. Dubey. 2007.'Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum'. Plant Cell Reports. 26 (11): 2027–2038.

Sharma, S.S., K.J. Dietz and T. Mimura. 2016. 'Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants'. Plant Cell Environ 39: 1112–1126.

Shaul, O., D.W. Hilgemann, J.J. de-Almeida-Engler, M. Van Montagu, D. Inzé and G. Galili. 1999. 'Cloning and characterization of a novel Mg²⁺/H⁺ exchanger'. EMBO J. 18: 3973–3980.

Singh, P., T.K. Mohanta and A.K. Sinha. 2015. 'Unraveling the intricate nexus of molecular mechanisms governing rice root development: OsMPK3/6 and auxin–cytokinin interplay'. PLoS ONE 10: e0123620.

Sinha, A.K., M. Jaggi, B. Raghuram and N. Tuteja. 2011.' Mitogen-activated protein kinase signaling in plants under abiotic stress'. Plant Signal Behav, 6: 196–203. 

Smeets, K., K. Opdenakker, T. Remans, C. Forzani, H. Hirt, J. Vangronsveld and A. Cuypers. 2013. 'The role of the kinase OXI1 in cadmium- and copper-induced molecular responses in Arabidopsis thaliana'. Plant Cell Environ. 36: 1228–1238.

Smirnov, O.E., A.M. Kosyan, O.I. Kosyk and N.Y. Taran. 2014. 'Buckwheat stomatal traits under aluminum toxicity.' Modern Phytomorphology, 6: 15–18.

Soda, N., A. Sharan, B.K. Gupta, S.L. Singla-Pareek, and A. Pareek. 2016. 'Evidence for nuclear interaction of a cytoskeleton protein (OsIFL) with metallothionein and its role in salinity stress tolerance'. Sci Rep. 6:34762.

Steinhorst, L. and J. Kudla. 2014. 'Signaling in cells and organisms–calcium holds the line'. Curr Opin Plant Biol. 22: 14–21.

Tamura, H., M. Honda, T. Sato and H. Kamachi. 2005. 'Pb hyperaccumulation and tolerance in common buckwheat (Fagopyrum esculentum Moench)'. J Plant Res. 118: 355–359.

Tao, P., X. Zhong, B. Li, W. Wang, Z. Yue, J. Lei, W. Guo and X. Huang. 2014 'Genome-wide identification and characterization of aquaporin genes (AQPs) in Chinese cabbage (Brassica rapa ssp. pekinensis)'. Mol Genet Genom, 289: 1131–1145.

Thomine, S., R. Wang, J.M. Ward, N.M. Crawford and J.I. Schroeder. 2000. 'Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes'. Proc Natl Acad Sci. USA 97: 4991–4996.

Tripathi, D.K., V.P. Singh, S.M. Prasad, D.K. Chauhan, N.K. Dubey and A.K. Rai. 2015. 'Silicon-mediated alleviation of Cr (VI) toxicity in wheat seedlings as evidenced by chlorophyll florescence, laser induced breakdown spectroscopy and anatomical changes'. Ecotoxicol Environ Saf. 113: 133–144.

Turchi, A., I. Tamantini, A.M. Camussi and M.L. Racchi. 2012. 'Expression of a metallothionein A1 gene of Pisum sativum in white poplar enhances tolerance and accumulation of zinc and copper'. Plant Sci. 183: 50–56.

Tyerman, S.D., H.U. Bohnert ,C. Maurel, E. Steudle and J.A. Smith. 1999. 'Plant aquaporins: their molecular biology, biophysics and significance for plant water relations'. J Exp Bot. 50: 1055–1071.

Usha, B., V. Gayatri, G. Suja and P. Ajay.2014. 'Melllothioneins from a hyperaccumulating plant Prosopis juliflora shows difference in heavy metal accumulation in transgenic tobacco'. Int J Agri Env Biotecnol. 7 (2): 241-246.

Usha, B., N.S. Keeran, M. Harikrishnan, K. Kavitha and A. Parida. 2011. 'Characterization of a type 3 metallothionein isolated from Porteresia coarctata.' Biol Plantarum, 55(1): 119–124.

Van De Mortel, J.E., H. Schat and P. D. Moerland. 2008.'Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens'. Plant Cell Environ. 31 (3): 301–324.

van de Mortel, J.E., L.A. Villanueva, H. Schat, J. Kwekkeboom, S. Coughlan, P.D. Moerland, E.V.L. van Themaat, M. Koornneef and M.G.M. Aarts. 2006. 'Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens'. Plant Physiol. 142(3): 1127–1147.

Vitti, A., M. Nuzzaci, A. Scopa, G. Tataranni, T. Remans, J. Vangronsveld and A. Sofo. 2013. 'Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with Cucumber mosaic virus (CMV) or exposed to cadmium'. Int J Mol Sci. 14: 6889–6902.  

Wang, S., Y. Zhang, Q. Song, Z. Fang, Z. Chen,Y. Zhang, L. Zhang, N. Niu, S. Ma, J. Wang, Y. Yao, Z. Hu and G. Zhang. 2018. 'Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat'. Front Plant Sci. 8:2217. 

Weaver, C.D., B. Crombie, G. Stacey and D.M. Roberts. 1991. 'Calcium-dependent phosphorylation of symbiosome membrane proteins from nitrogen-fixing soybean nodules: Evidence for phosphorylation of nodulin-26'. Am Soc Plant Physiol. 95: 222–227.

Xiong, L. and J.K. Zhu. 2002. 'Molecular and genetic aspects of plant responses to osmotic stress'. Plant Cell Environ, 25: 131–139.

Xue, T.T, X.Z. Li, W. Zhu, C.A. Wu, G.D. Yang, and C.C. Zheng. 2009. 'Cotton metallothionein GhMT3a, a reactive oxygen species scavenger increased tolerance against abiotic stress in transgenic tobacco and yeast'. J Exp Bot. 60: 339–349. 

Yamamoto, Y., Y. Kobayashi and H. Matsumoto. 2001. 'Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in Pea roots'. Plant Physiol. 125: 199-208.

Yang, J.L., Y.C. Wang, G.F. Liu, C.P. Yang and C.H. Li. 2011.'Tamarix hispida metallothionein-like ThMT3, a reactive oxygen species scavenger, increases tolerance against Cd²⁺, Zn²⁺, Cu²⁺, and NaCl in transgenic yeast'. Mol Biol Rep. 38: 1567–1574.

Yang, Z. and C. Chu. 2011. 'Towards understanding plant response to heavy metal stress'. In: Shanker A, Venkateswarlu B (ed). Agricultural and Biological Sciences: Abiotic Stress in Plants ‐ Mechanisms and Adaptations, pp 59‐78.

Yazaki, K. 2006. 'ABC transporters involved in the transport of plant secondary metabolites'. FEBS Letters, 580: 1183–1191.

Ye, Q., J. Muhr and E. Steudle. 2005. 'A cohesion/tension model for the gating of aquaporins allows estimation of water channel pore volumes in Chara'. Plant Cell Environ. 28: 525–535.

Yeh, C.M., P.S. Chien and H.J. Huang. 2007. 'Distinct signaling pathways for induction of MAP kinase activities by cadmium and copper in rice roots'. J Exp Bot. 58: 659–671.

Yuan, J., D. Chen, Y. Ren, X. Zhang and J. Zhao. 2008. 'Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggests functions in root development and seed embryo germination of rice'. Plant Physiol. 146: 1637–1650.

Zanella, L., L. Fattorini, P. Brunetti, E. Roccotiello and L. Cornara. 2016. 'Overexpression of AtPCS1 in tobacco increases arsenic and arsenic plus cadmium accumulation and detoxification'. Planta, 243: 605–622.

Zhang, J., M. Zhang, S. Tian, L. Lu and M.J.I. Shohag . 2014. 'Metallothionein 2 (SaMT2) from Sedum alfredii Hance Confers Increased Cd Tolerance and Accumulation in Yeast and Tobacco'. PLoS ONE 9(7): e102750.

Zhang, S.J, J.F. Ma and H. Matsumoto. 1998. 'High aluminum resistance in buckwheat: I. Al induced specific secretion of oxalic acid from root tip tips'. Plant Physiol. 117: 745–751.

Zhang, W.H. and S.D. Tyerman. 1999.'Inhibition of water channels by HgCl₂ in intact wheat root cells'. Plant Physiol. 120(3):849-857.

Zhang, Y., Z. Wang, T. Chai, Z. Wen and H. Zhang. 2008. 'Indian mustard aquaporin improves drought and heavy metal resistance in tobacco'. Mol Biotechnol 40 (3): 280-292.

Zhang, Y.W., N.F.Y. Tam and Y.S. Wong. 2004. 'Cloning and characterization of type 2 metallothionein-like gene from a wetland plant, Typha latifolia'. Plant Sci 167: 869–877.

Zheng, S.J. 2010.'Crop production on acidic soils: overcoming aluminum toxicity and phosphorus deficiency'. Anal Bot. 106: 183–184.

Zhou, B., W. Yao, S. Wang, X. Wang and T. Jiang. 2014. 'The Metallothionein Gene, TaMT3, from Tamarix androssowii Confers Cd²⁺ Tolerance in Tobacco'. Int J Mol Sci.15: 10398-10409.

Zou, J., G. Wang, J. Ji, J. Wang and H. Wu. 2017. 'Transcriptional, physiological and cytological analysis validated the roles of some key genes linked Cd stress in Salix matsudana Koidz'. Environ Exp Bot. 134: 116-129.